Plasticity contributes to a fine‐scale depth gradient in sticklebacks’ visual system

The light environment influences an animal's ability to forage, evade predators, and find mates, and consequently is known to drive local adaptation of visual systems. However, the light environment may also vary over fine spatial scales at which genetic adaptation is difficult. For instance, in aquatic systems, the available wavelengths of light change over a few metres depth. Do animals plastically adjust their visual system to such small‐scale environmental light variation? Here, we show that in three‐spine stickleback (Gasterosteus aculeatus), opsin gene expression (an important determinant of colour vision) changes over a 2‐m vertical gradient in nest depth. By experimentally altering the light environment using light filters to cover enclosures in a lake, we found that opsin expression can be adjusted on a short time frame (weeks) in response to the local light environment. This is to our knowledge the smallest spatial scale on which visual adjustments through opsin expression have been recorded in a natural setting along a continuously changing light environment.     

Among‐lake reciprocal transplants induce convergent expression of immune genes in threespine stickleback

Geographic variation in parasite communities can drive evolutionary divergence in host immune genes. However, biotic and abiotic environmental variation can also induce plastic differences in immune function among populations. At present, there is little information concerning the relative magnitudes of heritable vs. induced immune divergence in natural populations. We examined immune gene expression profiles of threespine stickleback (Gasterosteus aculeatus) from six lakes on Vancouver Island, British Columbia. Parasite community composition differs between lake types (large or small, containing limnetic‐ or benthic‐like stickleback) and between watersheds. We observed corresponding differences in immune gene expression profiles among wild‐caught stickleback, using a set of seven immune genes representing distinct branches of the immune system. To evaluate the role of environmental effects on this differentiation, we experimentally transplanted wild‐caught fish into cages in their native lake, or into a nearby foreign lake. Transplanted individuals' immune gene expression converged on patterns typical of their destination lake, deviating from their native expression profile. Transplant individuals' source population had a much smaller effect, suggesting relatively weak genetic underpinning of population differences in immunity, as viewed through gene expression. This strong environmental regulation of immune gene expression provides a counterpoint to the large emerging literature documenting microevolution and genetic diversification of immune function. Our findings illustrate the value of studying immunity in natural environmental settings where the immune system has evolved and actively functions.     

A field reciprocal transplant experiment reveals asymmetric costs of migration between lake and river ecotypes of three‐spined sticklebacks (Gasterosteus aculeatus)

Theory of local adaptation predicts that nonadapted migrants will suffer increased costs compared to local residents. Ultimately this process can result in the reduction of gene flow and culminate in speciation. Here, we experimentally investigated the relative fitness of migrants in foreign habitats, focusing on diverging lake and river ecotypes of three‐spined sticklebacks. A reciprocal transplant experiment performed in the field revealed asymmetric costs of migration: whereas mortality of river fish was increased under lake conditions, lake migrants suffered from reduced growth relative to river residents. Selection against migrants thus involved different traits in each habitat but generally contributed to bidirectional reduction in gene flow. Focusing particularly on the parasitic environments, migrant fish differed from resident fish in the parasite community they harboured. This pattern correlated with both cellular phenotypes of innate immunity as well as with allelic variation at the genes of the major histocompatibility complex. In addition to showing the costs of migration in three‐spined sticklebacks, this study highlights the role of asymmetric selection particularly from parasitism in genotype sorting and in the emergence of local adaptation.     

Assessing reproductive isolation using a contact zone between parapatric lake‐stream stickleback ecotypes

Ecological speciation occurs when populations evolve reproductive isolation as a result of divergent natural selection. This isolation can be influenced by many potential reproductive barriers, including selection against hybrids, selection against migrants and assortative mating. How and when these barriers act and interact in nature is understood for relatively few empirical systems. We used a mark–recapture experiment in a contact zone between lake and stream three‐spined sticklebacks (Gasterosteus aculeatus, Linnaeus) to evaluate the occurrence of hybrids (allowing inferences about mating isolation), the interannual survival of hybrids (allowing inferences about selection against hybrids) and the shift in lake‐like vs. stream‐like characteristics (allowing inferences about selection against migrants). Genetic and morphological data suggest the occurrence of hybrids and no selection against hybrids in general, a result contradictory to a number of other studies of sticklebacks. However, we did find selection against more lake‐like individuals, suggesting a barrier to gene flow from the lake into the stream. Combined with previous work on this system, our results suggest that multiple (most weakly and often asymmetric) barriers must be combining to yield substantial restrictions on gene flow. This work provides evidence of a reproductive barrier in lake–stream sticklebacks and highlights the value of assessing multiple reproductive barriers in natural contexts.     

Gene expression remodelling and immune response during adaptive divergence in an African cichlid fish

Variation in gene expression contributes to ecological speciation by facilitating population persistence in novel environments. Likewise, immune responses can be of relevance in speciation driven by adaptation to different environments. Previous studies examining gene expression differences between recently diverged ecotypes have often relied on only one pair of populations, targeted the expression of only a subset of genes or used wild‐caught individuals. Here, we investigated the contribution of habitat‐specific parasites and symbionts and the underlying immunological abilities of ecotype hosts to adaptive divergence in lake–river population pairs of the cichlid fish Astatotilapia burtoni. To shed light on the role of phenotypic plasticity in adaptive divergence, we compared parasite and microbiota communities, immune response, and gene expression patterns of fish from natural habitats and a lake‐like pond set‐up. In all investigated population pairs, lake fish were more heavily parasitized than river fish, in terms of both parasite taxon composition and infection abundance. The innate immune response in the wild was higher in lake than in river populations and was elevated in a river population exposed to lake parasites in the pond set‐up. Environmental differences between lake and river habitat and their distinct parasite communities have shaped differential gene expression, involving genes functioning in osmoregulation and immune response. Most changes in gene expression between lake and river samples in the wild and in the pond set‐up were based on a plastic response. Finally, gene expression and bacterial communities of wild‐caught individuals and individuals acclimatized to lake‐like pond conditions showed shifts underlying adaptive phenotypic plasticity.     

Calcium and salinity as selective factors in plate morph evolution of the three-spined stickleback (Gasterosteus aculeatus)

Identifying the causal factors underlying natural selection remains a key challenge in evolutionary biology. Although the genetic basis for the plate morph evolution of three-spined stickleback (Gasterosteus aculeatus) is well described, the environmental variables that form the basis for different morphs are not understood. We measured the effects of dissolved calcium and salinity on the growth of sticklebacks with different plate morphs from Scotland and Poland. There was a significant interaction of calcium with plate morph for fish from both regions, with complete morph sticklebacks growing more slowly at low calcium concentrations and low morph sticklebacks showing divergent responses to calcium concentration. A Scottish anadromous population showed evidence of local adaptation to high salinity, which was independent of plate morph. Polish and Scottish populations diverged in their response to salinity, suggesting a difference in osmotic regulation. The results implicate a role for calcium in selecting for plate morph evolution in sticklebacks, possibly as a limiting element in skeletal growth.     

Environmental adaptations as windows on molecular evolution

Changes in gene regulation may play an important role in adaptive evolution, particularly during adaptation to a changing environment. However, little is known about the molecular mechanisms underlying adaptively significant variation in gene regulation. To address this question, we are using environmental adaptations in populations of a fish, Fundulus heteroclitus as a window into the molecular evolution of gene regulation. F. heteroclitus are found along the East Coast of North America, with populations distributed along a steep thermal gradient. At the extremes of the species range, populations have undergone local adaptation to their habitat temperatures. A variety of genes differ in their regulation between these populations. We have determined the mechanism responsible for changes in lactate dehydrogenase-B (Ldh-B) gene regulation. A limited number of mutations in the regulatory sequence of this gene result in changes in its expression. Both the phenotypic (increased LDH activity) and genotypic (changes in Ldh-B regulatory sequences) differences between populations have been shown to be affected by natural selection, rather than genetic drift. Therefore, even a small number of mutations within important regulatory sequences can provide evolutionarily significant variation and have an impact on environmental adaptation.     

Shared ancestral polymorphisms and chromosomal rearrangements as potential drivers of local adaptation in a marine fish

Gene flow has tremendous importance for local adaptation, by influencing the fate of de novo mutations, maintaining standing genetic variation and driving adaptive introgression. Furthermore, structural variation as chromosomal rearrangements may facilitate adaptation despite high gene flow. However, our understanding of the evolutionary mechanisms impending or favouring local adaptation in the presence of gene flow is still limited to a restricted number of study systems. In this study, we examined how demographic history, shared ancestral polymorphism, and gene flow among glacial lineages contribute to local adaptation to sea conditions in a marine fish, the capelin (Mallotus villosus). We first assembled a 490‐Mbp draft genome of M. villosus to map our RAD sequence reads. Then, we used a large data set of genome‐wide single nucleotide polymorphisms (25,904 filtered SNPs) genotyped in 1,310 individuals collected from 31 spawning sites in the northwest Atlantic. We reconstructed the history of divergence among three glacial lineages and showed that they probably diverged from 3.8 to 1.8 million years ago and experienced secondary contacts. Within each lineage, our analyses provided evidence for large N_e and high gene flow among spawning sites. Within the Northwest Atlantic lineage, we detected a polymorphic chromosomal rearrangement leading to the occurrence of three haplogroups. Genotype–environment associations revealed molecular signatures of local adaptation to environmental conditions prevailing at spawning sites. Our study also suggests that both shared polymorphisms among lineages, resulting from standing genetic variation or introgression, and chromosomal rearrangements may contribute to local adaptation in the presence of high gene flow.     

Determinants of hierarchical genetic structure in Atlantic salmon populations: environmental factors vs. anthropogenic influences

Disentangling the effects of natural environmental features and anthropogenic factors on the genetic structure of endangered populations is an important challenge for conservation biology. Here, we investigated the combined influences of major environmental features and stocking with non‐native fish on the genetic structure and local adaptation of Atlantic salmon (Salmo salar) populations. We used 17 microsatellite loci to genotype 975 individuals originating from 34 French rivers. Bayesian analyses revealed a hierarchical genetic structure into five geographically distinct clusters. Coastal distance, geological substrate and river length were strong predictors of population structure. Gene flow was higher among rivers with similar geologies, suggesting local adaptation to geological substrate. The effect of river length was mainly owing to one highly differentiated population that has the farthest spawning grounds off the river mouth (up to 900 km) and the largest fish, suggesting local adaptation to river length. We detected high levels of admixture in stocked populations but also in neighbouring ones, implying large‐scale impacts of stocking through dispersal of non‐native individuals. However, we found relatively few admixed individuals suggesting a lower fitness of stocked fish and/or some reproductive isolation between wild and stocked individuals. When excluding stocked populations, genetic structure increased as did its correlation with environmental factors. This study overall indicates that geological substrate and river length are major environmental factors influencing gene flow and potential local adaptation among Atlantic salmon populations but that stocking with non‐native individuals may ultimately disrupt these natural patterns of gene flow among locally adapted populations.     

Local adaptation in the monocarpic perennial Carlina vulgaris at different spatial scales across Europe

Spatial variation in environmental conditions can lead to local adaptation of plant populations, particularly if gene flow among populations is low. Many studies have investigated adaptation to contrasting environmental conditions, but little is known about the spatial scale of adaptive evolution. We studied population differentiation and local adaptation at two spatial scales in the monocarpic grassland perennial Carlina vulgaris. We reciprocally transplanted seedlings among five European regions (northwestern Czech Republic, central Germany, Luxembourg, southern Sweden and northwestern Switzerland) and among populations of different sizes within three of the regions. We recorded survival, growth and reproduction over three growing periods. At the regional scale, several performance traits and the individual fitness of C. vulgaris were highest if the plants were grown in their home region and they decreased with increasing transplant distance. The effects are likely due to climatic differences that increased with the geographical distance between regions. At the local scale, there were significant interactions between the effects of the population of origin and the transplant site, but these were not due to an enhanced performance of plants at their home site and they were not related to the geographical or environmental distance between the site of origin and the transplant site. The size of the population of origin did not influence the strength of local adaptation. The results of our study suggest that C. vulgaris consists of regionally adapted genotypes, and that distance is a good predictor of the extent of adaptive differentiation at large scales ( > 200 km) but not at small scales. We conclude that patterns of local adaptation should be taken into account for the efficient preservation of genetic resources, when assessing the status of a plant species and during conservation planning.Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Local adaptation to salinity in the three‐spined stickleback?

Different lines of evidence suggest that the occurrence and extent of local adaptation in high gene flow marine environments – even in mobile and long‐lived vertebrates with complex life cycles – may be more widespread than earlier thought. We conducted a common garden experiment to test for local adaptation to salinity in Baltic Sea sticklebacks (Gasterosteus aculeatus). Fish from three different native salinity regimes (high, mid and low) were subjected to three salinity treatments (high, mid and low) in a full‐factorial experimental design. Irrespective of their origin, fish subjected to low (and mid) salinity treatments exhibited higher juvenile survival, grew to largest sizes and were in better condition than fish subjected to the high salinity treatment. However, a significant interaction between native and treatment salinities – resulting mainly from the poor performance of fish native to low salinity in the high salinity treatment – provided clear cut evidence for adaptation to local variation in salinity. Additional support for this inference was provided by the fact that the results concur with an earlier demonstration of significant differentiation in a number of genes with osmoregulatory functions across the same populations and that the population‐specific responses to salinity treatments exceeded that to be expected by random genetic drift.     

Limited evolutionary rescue of locally adapted populations facing climate change

Dispersal is a key determinant of a population''s evolutionary potential. It facilitates the propagation of beneficial alleles throughout the distributional range of spatially outspread populations and increases the speed of adaptation. However, when habitat is heterogeneous and individuals are locally adapted, dispersal may, at the same time, reduce fitness through increasing maladaptation. Here, we use a spatially explicit, allelic simulation model to quantify how these equivocal effects of dispersal affect a population''s evolutionary response to changing climate. Individuals carry a diploid set of chromosomes, with alleles coding for adaptation to non-climatic environmental conditions and climatic conditions, respectively. Our model results demonstrate that the interplay between gene flow and habitat heterogeneity may decrease effective dispersal and population size to such an extent that substantially reduces the likelihood of evolutionary rescue. Importantly, even when evolutionary rescue saves a population from extinction, its spatial range following climate change may be strongly narrowed, that is, the rescue is only partial. These findings emphasize that neglecting the impact of non-climatic, local adaptation might lead to a considerable overestimation of a population''s evolvability under rapid environmental change.     

GENE FLOW AND SELECTION ON PHENOTYPIC PLASTICITY IN AN ISLAND SYSTEM OF RANA TEMPORARIA

Gene flow is often considered to be one of the main factors that constrains local adaptation in a heterogeneous environment. However, gene flow may also lead to the evolution of phenotypic plasticity. We investigated the effect of gene flow on local adaptation and phenotypic plasticity in development time in island populations of the common frog Rana temporaria which breed in pools that differ in drying regimes. This was done by investigating associations between traits (measured in a common garden experiment) and selective factors (pool drying regimes and gene flow from other populations inhabiting different environments) by regression analyses and by comparing pairwise F_ST values (obtained from microsatellite analyses) with pairwise Q_ST values. We found that the degree of phenotypic plasticity was positively correlated with gene flow from other populations inhabiting different environments (among‐island environmental heterogeneity), as well as with local environmental heterogeneity within each population. Furthermore, local adaptation, manifested in the correlation between development time and the degree of pool drying on the islands, appears to have been caused by divergent selection pressures. The local adaptation in development time and phenotypic plasticity is quite remarkable, because the populations are young (less than 300 generations) and substantial gene flow is present among islands.     

Evidence of concurrent local adaptation and high phenotypic plasticity in a polar microeukaryote

Here we investigated whether there is evidence of local adaptation in strains of an ancestrally marine dinoflagellate to the lacustrine environment they now inhabit (optimal genotypes) and/or if they have evolved phenotypic plasticity (a range of phenotypes). Eleven strains of Polarella glacialis were isolated and cultured from three different environments: the polar seas, a hyposaline and a hypersaline Antarctic lake. Local adaptation was tested by comparing growth rates of lacustrine and marine strains at their own and reciprocal site conditions. To determine phenotypic plasticity, we measured the reaction norm for salinity. We found evidence of both, limited local adaptation and higher phenotypic plasticity in lacustrine strains when compared with marine ancestors. At extreme high salinities, local lake strains outperformed other strains, and at extreme low salinities, strains from the hyposaline lake outperformed all other strains. The data suggest that lake populations may have evolved higher phenotypic plasticity in the lake habitats compared with the sea, presumably due to the high temporal variability in salinity in the lacustrine systems. Moreover, the interval of salinity tolerance differed between strains from the hyposaline and hypersaline lakes, indicating local adaptation promoted by different salinity.